'True' and 'Look-Alike' Deviance Detection in Primary Auditory Cortex of the Macaque

Teichert, T.

University of Pittsburgh, Department of Psychiatry and Bioengineering

Deviance detection (DD), i.e., increased neural activity to stimuli that violate expectations, can facilitate the identification and processing of informative events. While 'true' DD requires forming expectations and detecting deviations from them, functionally similar neural responses may be generated by basic stimulus-specific adaptation (SSA). Here we studied responses of primary auditory cortex (A1) in awake monkeys to tones that either violated expectations or were embedded in sequences that prevented the formation of expectations. Identical sequences were presented to a computational model of SSA based on short-term synaptic plasticity in thalamic afferents. Together, this determined whether A1 indeed responds stronger to stimuli that violate expectations and whether these responses are compatible with SSA or require a more complex explanation such as 'true' DD.

Following standard conventions, DD was operationalized as stronger responses for deviants in the regular compared to the random condition. Based on this definition both animals exhibited DD. This is the first report of DD in this species. DD was strongest in layers 3 and 5, but also present in layer 4. While DD is believed to be the epitome of a phenomenon that can not be explained by SSA, our SSA-model readily replicated this finding if it used biologically realistic values of vesicle release probability and a plausible receptive field structure that we describe as 'uniform pedestal plus center'. Thus, short-term synaptic plasticity in combination with a simple yet effective local circuit architecture can enable A1 to generate a DD 'look-alike' that can facilitate the processing of informative stimuli just as effectively as true DD, but with less computational overhead. However, the SSA-model failed to capture observed differences in timing between DD and SSA. This leaves the door open to the speculation that monkey A1 also exhibits true DD in addition to the DD look-alike.